University of Plymouth PEARL https://pearl.plymouth.ac.uk Faculty of Science and Engineering School of Biological and Marine Sciences 2019-05-09 Preferential parasitism of native oyster Ostrea edulis over non-native Magallana gigas by a Polydorid worm Lemasson, A http://hdl.handle.net/10026.1/13631 10.1007/s12237-019-00560-y Estuaries and Coasts Springer Verlag All content in PEARL is protected by copyright law. Author manuscripts are made available in accordance with publisher policies. Please cite only the published version using the details provided on the item record or document. In the absence of an open licence (e.g. Creative Commons), permissions for further reuse of content should be sought from the publisher or author. 1 Preferential parasitism of native oyster Ostrea edulis over non-native 2 Magallana gigas by a Polydorid worm 3 4 Lemasson A.J.a* and A.M. Knightsa 5 6 a Marine Biology and Ecology Research Centre, School of Biological and Marine 7 Sciences, University of Plymouth, Drake Circus, Plymouth, PL4 8AA. UK 8 *Corresponding Author: A.J. Lemasson ([email protected]) 9 10 Abstract 11 Parasites are important structural components of marine communities that can affect 12 organism fitness and ecological interactions, and the provision of ecosystem services. 13 Here, we investigate the host association of Polydora ciliata with two ecologically and 14 economically important oyster species (Ostrea edulis; Magallana gigas) and examine 15 its impacts on two fitness aspects: condition and shell strength. Our results provide 16 strong inferential evidence of host-specificity by P. ciliata with a tendency toward 17 infestation of the native O. edulis over the introduced M. gigas. Evidence suggests 18 increasing prevalence of parasitism with organismal age, but no clear indication that 19 parasitism leads to reduced condition or shell strength. The prevalence of infection of 20 O. edulis by P. ciliata over M. gigas observed here holds potential implications for 21 species competition and dominance, and their respective population maintenance, 22 which could explain the much lower abundances of O. edulis compared to M. gigas at 23 specific geographical locations. Additionally, these results hold significance for the 24 aquaculture sector, with parasitism likely to lower production output and decrease the 25 end-product market value. 26 1 1 Keywords 2 Intertidal; Estuary; Ecological interactions; Non-native species; Aquaculture 3 2 1 Introduction 2 Parasites are increasingly recognised as important structural components of marine 3 communities (Firth et al. 2017). They modulate the ecology and biogeography of their 4 host-species, but also indirectly shape the whole community via coincidental effects 5 on the habitat and ecological interactions, particularly in the case of an ecosystem- 6 engineer host (Mouritsen and Poulin 2002). Taxa affected by parasitism include 7 mammals, teleosts (Hoberg and Brooks 2008), birds, molluscs and crustaceans 8 (Mouritsen and Poulin 2002). 9 10 Bivalves are known to be hosts for various parasites that live in their mantles or within 11 their shells (Blake and Evans 1973; Carroll et al. 2015; Diez et al. 2014; Sato-Okoshi 12 et al. 2012). Parasites, by definition, are harmful to their host to a certain degree. 13 Negative effects can vary from minor metabolic changes to more important soft tissue 14 damages (Mouritsen and Poulin 2002). The deleterious effects of Polydorid worms on 15 bivalve host species can vary with the intensity of infestation, but usually lead to 16 physiological deficiencies (Chambon et al. 2007), reduced condition (Ambariyanto and 17 Seed 1991; Chambon et al. 2007; Riascos et al. 2008), and reduced shell strength 18 (Bergman et al. 1982; Kent 1981; Korringa 1951). This in turn affects important 19 ecological and biological processes, such as predator-prey interactions (Ambariyanto 20 and Seed 1991) and behaviour (Riascos et al. 2008). 21 22 Increasingly, the implications of parasitism for the bivalve aquaculture industry are 23 being considered ( Clements et al., 2017; Diez et al. 2011; Royer et al. 2006; Simon 24 and Sato-Okoshi 2015), not least due to the negative economic and health 25 consequences parasitic infestation can cause. For example, parasites can cause the 3 1 formation of mud blisters (Blake and Evans 1973; Korringa 1952; Nell 2007) that affect 2 sensory and aesthetic parameters, reducing the quality of the product (Korringa 1951; 3 Lafferty et al. 2015) and negatively affecting the economic value, as well as acting as 4 a vector of disease (Lafferty et al. 2015; Powell et al. 2015). 5 6 In the UK, the native European flat oyster, Ostrea edulis, and the non-native invasive 7 Pacific oyster, Magallana gigas, are commercially valuable aquaculture species 8 (Lemasson et al. 2017). In addition, they are both ecosystem engineers (sensu Jones 9 et al. 1996) that provide numerous ecosystem services, such as reef formation, 10 erosion control, improvement of water quality and food provision (Herbert et al. 2012). 11 Although historically O. edulis was highly abundant in the UK (Orton 1937), their 12 continued decline has led to protection and extensive restoration programs (Woolmer 13 et al. 2011). In contrast, M. gigas continues to spread polewards facilitated by the 14 warming of sea surface waters (Rinde et al. 2016; Thomas et al. 2016; Townhill et al. 15 2017). In the Wadden Sea, there has been a gradual shift from native mussel beds to 16 invasive oyster beds following their introduction in 1986 (Kochmann et al. 2008), yet 17 recent studies have shown that both species can co-exist without detrimental 18 ecosystem impacts (Buschbaum et al. 2016; Reise et al. 2017). In Plymouth Sound 19 UK, mixed oyster beds of both O. edulis and M. gigas occur, but M. gigas are 20 increasingly prevalent (pers. observations). Although it is likely that some level of 21 competition for space and resources takes place, the ecological impact of M. gigas on 22 O. edulis remains unclear and may not alter associated assemblages (Zwerschke et 23 al. 2016). 24 4 1 Polydora ciliata, a parasitic worm affecting shellfish, has long been known to occur in 2 the South-West of the UK (Kent 1977) and in Plymouth waters, due to the occurrence 3 of Devonian limestone, a choice settlement substrate for the species (Dorsett 1961). 4 Oysters found along Plymouth Sound shores present signs of parasitism by Polydorid 5 worms (pers. observations), with a preference for O. edulis as the host species. To 6 date, the rate and prevalence of parasitism have not been reported, but based on 7 observations, it is hypothesised that parasitism may be in part responsible for the 8 reductions in abundance and high mortality of O. edulis (e.g. Naciri-Graven et al. 9 1998). If this is true, the physiological consequences of differential parasitism between 10 the two species of oysters could help to explain the abundance pattern observed, by 11 slowing the recovery of O. edulis and facilitating the spread of M. gigas, with important 12 ecological and economic outcomes. 13 14 Here, we investigated the host association of Polydora ciliata between Ostrea edulis 15 and Magallana gigas found in Plymouth Sound, UK, in relation to oyster size (proxy 16 for age), and examined if their condition index (tool widely used in the aquaculture 17 sector to evaluate the overall quality and health of bivalves (Knights, 2012; Marin et 18 al., 2003)) - and shell strength (indication of resistance to durophagous predators) 19 were affected. 20 21 Methods 22 ‘Large’ and ‘small’ (see size-specifications below) individuals of each species were 23 hand-collected at low tide during four sampling events through 2015-2016 (as part of 24 separate studies) from the same low-intertidal site in Plymouth Sound (50°23’29.95”N, 25 004°13’16.77”W). Organisms were randomly selected within the chosen size bracket 5 1 and brought back in buckets without seawater to the Marine Biology and Ecology 2 Research Centre at Plymouth University. ‘Large’ Magallana gigas were collected in 3 July 2015, ‘large’ Ostrea edulis in January 2016, ‘small’ M. gigas in August 2016, and 4 ‘small’ O. edulis in November 2016. The average duration of each sampling event 5 varied between one (for M. gigas) and two (for O. edulis) hours. 6 The maximum dorso-ventral length of each individual was measured to the nearest 7 millimetre using Vernier callipers (Mitutoya, Japan). Each individual was categorized 8 as being either ‘small’ (<70 mm in length for O. edulis; <100 mm in length for M. gigas) 9 or ‘large’ (>70 mm in length for O. edulis; >100 mm in length for M. gigas) before being 10 destructively sampled to assess the degree of parasitism by Polydora ciliata using 11 macroscopic examination of the inside and outside of the valves. Oyster parasitism 12 was described using one of three possible infection-level categorical classifications: 13 uninfected (no visible sign of infection), infected low-level (less than 10 visible 14 burrows), or infected high-level (more than 10 visible burrows) (Supplementary Figure 15 1). Differences in worm infection between species and between size classes within 16 species were assessed using a contingency table and �2 test of association. 17 18 The condition index (CI) of 20 randomly selected individuals from each species was 19 determined following the method recommended by Lucas and Beninger (1985): CI = 20 (dry meat weight / dry shell weight) × 100. Dry tissue weight and dry shell weight were 21 determined after each oyster was shucked using an oyster knife and oven-dried at 22 105°C in pre-weighed aluminium trays for up to 48h. Tissues were considered 'dry' 23 after three successive measurements of the same mass. As nearly 100% of O.